Polyphasic Fluorescence Lazar - 2006a PDF

CSIRO PUBLISHING
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Functional Plant Biology, 2006, 33, 930
Review: The polyphasic chlorophyll a uorescence rise measured under high intensity of exciting light
Du san Laz ar
Palack y University, Faculty of Science, Department of Experimental Physics, Laboratory of Biophysics, t r. Svobody 26, 771 46 Olomouc, Czech Republic. Email: lazard@seznam.cz Abstract. Chlorophyll a uorescence rise caused by illumination of photosynthetic samples by high intensity of exciting light, the OJIP (OI1 I2 P) transient, is reviewed here. First, basic information about chlorophyll a uorescence is given, followed by a description of instrumental set-ups, nomenclature of the transient, and samples used for the measurements. The review mainly focuses on the explanation of particular steps of the transient based on experimental and theoretical results, published since a last review on chlorophyll a uorescence induction [Laz ar D (1999) Biochimica et Biophysica Acta 1412, 128]. In addition to old concepts (e.g. changes in redox states of electron acceptors of photosystem II (PSII), effect of the donor side of PSII, uorescence quenching by oxidised plastoquinone pool), new approaches (e.g. electric voltage across thylakoid membranes, electron transport through the inactive branch in PSII, recombinations between PSII electron acceptors and donors, electron transport reactions after PSII, light gradient within the sample) are reviewed. The K-step, usually detected after a high-temperature stress, and other steps appearing in the transient (the H and G steps) are also discussed. Finally, some applications of the transient are also mentioned. Keywords: uorescence induction, G step, H step, K step, model, OJIP (OI1 I2 P) transient, theory.
I Chlorophyll a uorescence and the F0 and FM levels The quantum yield of chlorophyll (Chl) a uorescence in a solution (where excitation energy transfer and photochemistry do not occur) is 2035% (Latimer et al. 1956; Weber and Teale 1957) and this uorescence has a lifetime of 620 ns (M uller et al. 1969; Avarmaa et al. 1977; Pfarrherr et al. 1991; Brody 2002). In contrast, the quantum yield of Chl a uorescence from the photosynthetic apparatus is only 28% (from open to closed reaction centres of photosystem II, RCII; Latimer et al. 1956; Trissl et al. 1993) with an average lifetime of 300 ps (for open RCII; Keuper and Sauer 1989; Marder and Raskin 1993; Briantais et al. 1996; Gilmore et al. 1996) and 1.6 ns (for closed RCII; Keuper and Sauer 1989; Marder and Raskin 1993; Brody 2002). Under physiological conditions, uorescence signal during uorescence rise (FLR) is assumed to originate mainly from photosystem II (PSII) [reviewed by Govindjee et al. (1986); Krause and Weis (1991); Dau (1994)]. Contribution of photosystem I (PSI) to the overall uorescence signal during FLR at room temperature is 1520% (Strasser and Butler 1977; Wong and Govindjee 1979; Stahl et al. 1989; Roelofs et al. 1992; Trissl et al. 1993)
Abbreviations used: See Table 1 for a complete list of abbreviations used. CSIRO 2006
and its uorescence is assumed to have a constant level; uorescence from PSI contributes only to minimal uorescence, F0 , [however, see also Ikegami (1976) and Byrdin et al. (2000); section II.4.2.10]. But at emission wavelengths greater than 700 nm the contribution of the PSI uorescence to F0 can be up to 3055% (Pf undel 1998; Gilmore et al. 2000; Franck et al. 2002). Nevertheless, in a rst approximation, which is well accepted in photosynthesis research, FLR is understood to originate from PSII. Minimal uorescence, F0 , is dened as the uorescence when all RCIIs are open, i.e. when the rst quinone electron acceptor of PSII, QA , is oxidised [see also Vredenberg (2000); Strasser and Stirbet (2001), and section II.4.2.3 for alternative approaches]. As Butler (1977, 1978) postulated that every uorescence signal comes from Chls of light harvesting antennae (LHA), F0 is the uorescence signal coming from excited Chls of LHA before the excitations reach RCII (Mathis and Paillotin 1981). Owens (1996) suggested that F0 level is a consequence of the transfer equilibrium: an equilibrium between the formation of the excited states among all the light harvesting pigments and P680 and utilisation of the excited states for reversible
10.1071/FP05095
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Table 1. List of abbreviations used in the text Abbreviation A515 , A520 ADRY Chl CP43, CP47 cyt DBMIB DCMU DF F0 FI FI FJ FK FLR FM FNR FP FV FV / FM HQ LED LHA LHCII MCA MV NADP NH2 OH O, K, J ( I1 i), I ( I2 ), H, G, P OEC P680 3 P680* P700 PAM PBQ PC PEA Pheo Pheo2 PQ PSI PSII Q2 QA QB RCII RRP Rubisco Si (i = 0, 1, 2, 3) T820 TMPD Tris TSTM VI VJ YZ
A
Denition Absorbance signal measured at 515 or 520 nm, respectively Accelerator of the deactivation reactions of the enzyme Y in OEC Chlorophyll A 43-kDa, 47-kDa Chl containing inner LHAs of PSII Cytochrome 2,5-dibromo-3-methyl-6-isopropyl-p-bezoquinone 3-(3 ,4 -dichlorophenyl)-1,1-dimethylurea; diuron Delayed uorescence Minimal Chl a uorescence Chl a uorescence induction (both the FLR and uorescence decay) Chl a uorescence signal at the I step in FLR measured under high intensity of exciting light Chl a uorescence signal at the J step in FLR measured under high intensity of exciting light Chl a uorescence signal at the K step in FLR measured under high intensity of exciting light Chl a uorescence rise Maximal Chl a uorescence Ferredoxin-NADP+ oxidoreductase Fluorescence parameter Variable uorescence (= FM F0 ) Maximal quantum yield of PSII photochemistry 1,4-benzenediol; hydroquinone Light-emitting diode Chl containing light harvesting antenna(e) Chl containing light harvesting complex of PSII Metabolic control analysis Methylviologen Nicotinamide adenine dinucleotide phosphate Hydroxylamine Particular steps in FLR measured under high intensity of exciting light Oxygen-evolving complex Primary electron donor in PSIIA Triplet excited state of P680 Primary electron donor in PSIA Pulse amplitude modulation 1,4-benzenedione; p-benzoquinone Plastocyanin Plant efciency analyser Primary electron acceptor in PSII, pheophytin, localised in D1 protein Pheophytin localised in D2 protein Plastoquinone Photosystem I Photosystem II A component of PSII The rst quinone electron acceptor in PSII The second quinone electron acceptor in PSII Reaction centre of PSII Reversible radical pair Ribulose-1,5-bisphosphate carboxylase / oxygenase S-states of OEC Transmission signal measured at 820 nm N,N,N ,N -tetramethyl-p-phenylenediamine Tris(hydroxymethyl)aminomethane Three-state trapping model Relative variable uorescence at the I step Relative variable uorescence at the J step Tyrosine 161 of D1 protein
What is denoted as P680 and P700 is generally thought to be the primary electron donors in PSII and PSI, respectively, but recent results indicate that the primary electron donors in both PSII and PSI are probably accessory chlorophylls and not P680 and P700, respectively. For more details see van Mourik (2004), Novoderezhkin et al. (2005), and Groot et al. (2005) for PSII and M uller et al. (2003) and Holzwarth et al. (2005a, b) for PSI.
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primary photochemistry (i.e. charge separation and charge recombination; Laible et al. 1994; see also Laz ar 2003). Maximal uorescence FM is dened as the uorescence when all the RCIIs are closed, i.e. when all QA is reduced (Vredenberg 2000; Strasser and Stirbet 2001, and section II.4.2.3 for alternative approaches). Even if charge separation (i.e. formation of P680+ Pheo from P680*Pheo) can occur in the closed RSII, its rate constant is 36 times smaller [see Laz ar (2003) for a summary of the rate constants according to different authors] than in the case of open RCII. Further, in the case of the closed RCII, the rate constant of the charge recombination (i.e. formation of P680*Pheo from P680+ Pheo ) is higher than in the case of open RCII. The changes in the rate constants of the charge separation and recombination lead to increased accumulation (lifetime) of the excited states in the closed RCII when compared with open RCII; this leads to higher uorescence emission in the closed RCII than in the open RCII. II The polyphasic chlorophyll a uorescence rise: OJIP (OI1 I2 P) transient The OJIP (OI1 I2 P) FLR is reviewed in this section. A summary of the instrumental set-ups for the measurement of the FLR is given rst, followed by a description of the nomenclature used for the FLR and of the samples used for the measurements. Finally, particular steps of the FLR are explained in detail. Additional information can be found in related reviews (Govindjee et al. 1986; Krause and Weis 1991; Dau 1994; Govindjee 1995; Joshi and Mohanty 1995; Mohammed et al. 1995; Schreiber et al. 1995; Laz ar 1999; ek and Bart Roh ac ak 1999; Samson et al. 1999; Chaerle and Van Der Straeten 2000, 2001; Maxwell and Johnson 2000; ek 2002; Sayed 2003; Baker and Rosenqvist 2004; Roh ac Oxborough 2004a). Readers are also referred to a recently published book Chlorophyll a uorescence: a signature of photosynthesis (Papageorgiou and Govindjee 2004), in which the state of the art, related to the FLR, is reviewed extensively (e.g. Govindjee 2004; Schreiber 2004; Strasser et al. 2004; Vredenberg 2004). II.1 Instrumental set-ups Three conditions must be guaranteed by an experimental set-up to measure and distinguish the polyphasic FLR: a high (saturating) intensity of exciting light (300010000 mol photons m2 s1 ), a fast beginning of illumination of a sample, and a fast time resolution of detected uorescence signal. The rst condition is realised by high intensity light sources (halogen and xenon lamps, light emitting diodes, lasers) and the second condition by using a fast enough shutter or shutter-less set-up. A fast enough analogue / digital converter must be used to ensure a satisfactory time resolution of the detected uorescence signal.
The rst results on the measurements of the FLR under high intensity of excited light were published by Morin (1964) and Delosme (1967). Both these investigators used laboratory made set-up where a fast enough shutter was realised by using a gun whose 22 long rie bullet blew apart a metal plate that was between the sample and the illuminating xenon lamp, serving as a light source. More user-friendly instruments and commercial uorometers have recently replaced such a dangerous set-up. Ruth (1990, 1991) used a laboratory-made uorometer with a heliumneon laser as a light source and acousto-optic modulator (Bragg cell) as a shutter, ensuring a fast enough beginning of the illumination, to measure the FLR. However, the laser used by Ruth did not provide a sufciently high intensity of exciting light. Another laboratory-made uorometer was used for the il and Dau (2000, 2002). measurement of the FLR by Posp s In this uorometer, light emitting diodes (LED) were used as a light source, which also ensures a fast beginning of the illumination. Ulrich Schreiber and co-workers (Schreiber 1986; Schreiber et al. 1986; Schreiber and Neubauer 1987; Neubauer and Schreiber 1987) published the rst measurements of the FLR under high intensity of exciting light, using a commercial uorometer (Pulse Amplitude Modulation, PAM 101103; Walz, Germany) where a halogen lamp serves as a light source and a mechanical shutter (full shutter opening within 800 s) ensures a fast beginning of the illumination. In 1991 and 1992 the rst FLR measurements with another commercial uorometer, the PEA (Plant Efciency Analyser; Hansatech, England) uorometer were published by Strasser and Govindjee (1991, 1992). There is no shutter in the PEA uorometer and a fast enough beginning of the illumination and the illumination itself is achieved by LEDs. The same set-up for the measurement of the FLR is also used by the DoubleModulation Fluorometer (Photon Systems Instruments, Brno, Czech Republic). This uorometer even enables measurements of the FLR with time resolution of 100 ns during extremely strong (200 000 mol photons m2 s1 ) short (up to 50100 s) saturating light ash, the socalled ash uorescence induction (Nedbal et al. 1999; ek et al. 2001). Kobl z The uorometers most often used for the measurements of the FLR, the PAM and PEA uorometers, however, use different approaches for the detection of uorescence signal. In the PEA uorometer, continuous illumination of a sample is used to induce photosynthetic electron transport (i.e. as actinic light), but also serves to assess the state of a sample via its uorescence signal (i.e. as measuring light). In the PAM 101103 uorometer, pulse-modulated measuring light and continuous actinic light are separated. Hence, photosynthetic electron transport (and closure of RCIIs) is induced by continuous illumination, but the state of the sample is probed by short (1 s) measuring light
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ashes placed 10 s apart (during the FLR measurement). By measuring the uorescence signal during each individual measuring ash as well as a few microseconds thereafter and then subtracting the two signals, the uorescence excited by the actinic light is eliminated. Therefore, as intensity of the measuring light is constant, PAM uorometers measure uorescence yield, irrespective of the uorescence intensity excited by actinic illumination. Fluorescence yield may vary by about a factor of ve (between all RCIIs being open or closed), whereas there is no limit for uorescence intensity, as it is proportional to intensity of excitation light. The different approaches used by PAM and PEA uorometers for the measurements are reected in the way the F0 level is measured or calculated. In the PEA uorometer, the F0 level is not measured but calculated from experimental data; FLR data points in the range of 80120 s are tted by a linear function and then extrapolated to time zero, whose uorescence signal is considered as the F0 level. The F0 level determined in this way is within 10% of the uorescence signal measured at 4050 s of the FLR (e.g. Strasser et al. 1995; Su sila et al. 2004). Therefore, the FLRs measured by PEA uorometer are usually presented starting from 4050 s (the O level). Using different Chl concentrations (acetone extracts, where excitation energy transfer and photochemistry do not occur) and sample thicknesses, Su sila et al. (2004) pointed out that the uorescence signal detected by the PEA uorometer, is distorted by the uorometer up to 50 s but starting from this time to the end of the measurement period, the detected
uorescence signal is constant. In contrast, the PAM 101103 uorometer measures the F0 level by the measuring ashes before the onset of actinic illumination. Although the energy of the individual measuring ashes is very high, their short duration and repetition with enough time between two ashes (625 s for the F0 measurement) ensure that integral energy of measuring ashes is very small and does not cause any signicant photochemical electron transport in the sample. However, it is necessary to establish that true F0 is being measured by checking it at decreased light intensity of the measuring ashes. II.2 Nomenclature All steps in the FLR can be clearly revealed only when logarithmic presentation of time axis is used. In the following text, the term step is used for a hump or a wave or a peak that appears visually at a given time in the FLR. A transient or a phase is used in the following text as a part of the FLR that starts at a step and is completed in another step. The J (I1 ) and I (I2 ) steps usually appear at 23 ms and 3050 ms, respectively (see Fig. 1A, curve a). The O step stands for F0 and the P step represents FM usually reached at 200500 ms. The J and I notation of particular steps in the FLR is based on the original work by Strasser and Govindjee (1991, 1992). However, the two steps appearing between the F0 and FM levels were denoted earlier as I1 and I2 by U. Schreiber and co-workers (Schreiber 1986; Schreiber et al. 1986; Schreiber and Neubauer 1987; Neubauer and Schreiber 1987; see Fig. 1B). Strasser et al. (1995) established equivalencies between the J and I1 steps and the I and I2 steps
P I
a b I2
Fluorescence yield (r. u.)
M
4
Fluorescence intensity (relative units)
4 4 3 2 1 4 3 2 Log time (s) 1 2
I1
O
1
O
4 3 2 1 0
O
0.00 0.05 0.10 0.15
B
0.20
Log time (s)
Time (s)
Fig. 1. FLRs measured with dark-adapted barley leaves (part A; curve a, no treatment; curve b, leaf incubated in 32 mM DCMU solution for 5 h; data from Laz ar et al. 1998) and tobacco leaf (part B, no treatment; data from Laz ar 1999) by PEA and PAM uorometer, respectively, under high intensity of exciting light [3400 mol photons m2 s1 of red light (A) and 9000 mol photons m2 s1 of white light (B)]. The same curve as in main part B is presented on a logarithmic time-axis in the inset of part B. The O, J (I1 ), I (I2 ), and P (M) steps are labelled.
Fluorescence yield (relative units)
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since (i) the steps appear at the same time in the FLR (compare curve a in Fig. 1A and the inset in Fig. 1B) and (ii) the relative heights of the J and I1 steps on the one hand and of the I and I2 steps on the other hand have the same light intensity dependencies. Delosme (1967) denoted by the small letter i the only step he measured between F0 and FM at 2 ms; it seems to be equivalent to the J ( I1 ) step. As the FLR is now often measured by PEA, the OJIP notation is used in the text. As the initial OJ transient reects primary photochemical reactions (see below), it was called the photochemical phase of the FLR (Delosme 1967; Neubauer and Schreiber 1987; Strasser et al. 1995). The main feature of this phase is that the initial slope and relative height of the phase strongly depends on the intensity of the exciting light (see e.g. Strasser et al. 1995; Tomek et al. 2001). In contrast, subsequent JIP transient cannot be speeded up by further increase in the intensity of exciting light (see e.g. Strasser et al. 1995; Tomek et al. 2001) and it was called the thermal phase of the FLR (Delosme 1967; Neubauer and Schreiber 1987) because it depends on the temperature of measurement (within physiological range). Under certain conditions, additional steps, the K, G, and H steps, can appear in the FLR. These steps are described in detail later under separate sections. II.3 Samples Chlorophyll a uorescence rise can be measured with any photosynthetic organism, but it has been measured mostly with whole leaves, mosses, algae, cyanobacteria, chloroplasts, and thylakoid membranes. FLRs from these samples measured at room temperature are usually characterised by typical OJIP transients, as mentioned above (but see also section III.2). While a detailed explanation of the OJIP transient measured with these usual samples is given in the following section, a short description of measurements of the FLR with unusual samples and the results are briey summarised now. When the FLR is measured with PSII membranes, the il and Dau 2000, 2002; Heredia I step is not present (Posp s and De Las Rivas 2003). Exploration of the FLR measured with PSII membranes led to new suggestions for the origin of the particular steps in the FLR (see sections II.4.2.2 and II.4.2.12). Fluorescence quenching by the oxidised plastoquinone (PQ) pool (see section II.4.2.4 for more details) is more pronounced in PSII membranes than in more structurally organised samples (thylakoid membranes, chloroplasts, leaves) (Kurreck and Renger 1998; Kurreck il and Dau 2000, 2002). J. Kurreck and et al. 2000; Posp s co-workers (Kurreck and Renger 1998; Kurreck et al. 2000) explained this nding by greater afnity of PQ molecules for LHA to form a quenching complex in the case of PSII membranes than in the case of the more structurally organised samples.
The FLR was also measured with aggregates of light harvesting complex of PSII (LHCII) and with trimeric PSI to explore the generation of uorescence quenchers from the triplet states of chlorophyll (Barzda et al. 2000) and quantum yield of uorescence in PSI with initially reduced or oxidised primary electron donor in PSI, P700 (Byrdin et al. 2000; see also section II.4.2.10), respectively. II.4 Explanation In this section possible explanations of the particular steps in the OJIP FLR, suggested in the literature, are summarised, separately for the photochemical and thermal phases of the FLR. It seems that each of these explanations separately cannot explain particular steps of the FLR and probably all of the processes described below occur simultaneously and affect the steps of the FLR to some extent. II.4.1 The photochemical phase II.4.1.1 Accumulation of reduced QA being oxidised with QB
Duysens and Sweers (1963) had already proposed the existence of a quencher Q that was removed as Chl a uorescence rose. According to the suggestion by Delosme (1967), the photochemical phase (OJ transient) corresponds to the destruction of a quencher Q which is the primary reactant of the photoreaction II in photosynthesis. Using present notations, Q should be QA . In agreement with this suggestion, a working hypothesis was introduced by Strasser and Govindjee (1992) proposing that the J step reects light-driven accumulation of QA with QB , the second quinone electron acceptor in PSII, being oxidised, that is, J QA QB state. A main experimental proof that the OJ FLR represents accumulation of only reduced QA comes from measurements with 3-(3 ,4 -dichlorophenyl)-1,1-dimethylurea (DCMU), an inhibitor of electron transport between QA and PQ molecules of the PQ pool [Oettmeier and Soll 1983; Trebst and Draber 1986; Trebst 1987; Shigematsu et al. 1989; DCMU inhibits this reaction by binding to the QB pocket of PSII (Velthuys 1981)]. When a sample is treated with DCMU, the FLR measured at high intensity of exciting light is characterised by a steep uorescence increase, reaching maximal saturation level at approximately the position of the J step measured in the sample without DCMU (Strasser et al. 1995; Laz ar et al. 1998, 2001; Tomek et al. 2001; compare curves a and b in Fig. 1A). Theoretical simulations of the FLR either with or without DCMU also conrmed the suggestion that it is mainly QA that accumulates in the reduced state in the position of the J step (Stirbet and Strasser 1995a, b, 2001; Stirbet et al. 1995, il 1999; 1998; Laz ar et al. 1997b, 2005b; Laz ar and Posp s Strasser and Stirbet 2001; Tomek et al. 2001; Lebedeva et al. 2002; Laz ar 2003; Zhu et al. 2005). It is important to realise that when DCMU is not present, the QA may not be fully
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reduced in the J step of the FLR because electrons from QA are continuously transferred to QB and further on towards PSI. Therefore, when DCMU is not present, the J step may represent only a partial and not full accumulation of QA . II.4.1.2 The donor side of PSII Using different treatments (Tris, high temperature, ADRYreagents, NH2 OH, pH) that inhibit donor side of PSII, the photochemical phase of the FLR was shown to be partially controlled by the donor side of PSII (see e.g. Schreiber and Neubauer 1987; Bukhov et al. 2004). The conclusion that the donor side of PSII can affect the photochemical phase of the FLR was also made on the basis of measurement of the FLR under low intensity of exciting light (Hsu 1993; Lavergne and Leci 1993) and using the ash uorescence ek et al. 2001). However, the induction measurements (Kobl z effect of the donor side of PSII on photochemical phase of the FLR found by Hsu (1993) and Lavergne and Leci (1993) was determined on the basis of assumption of a different uorescence quenching in different redox states (the S-states) of oxygen evolving complex (OEC) and is therefore related to the donor side uorescence quenching and not to the rates of the S-state transitions of OEC as such. Also theoretical simulations of the FLR revealed an effect of the donor side on the photochemical phase of the FLR il 1999; Laz (Stirbet et al. 1998; Laz ar and Posp s ar 2003). As inhibition of the donor side of PSII results in appearance of the K step in the FLR, the effect of the donor side of PSII on the FLR is discussed more extensively in section III.1. II.4.1.3 Excitation energy transfer among PSIIs Theoretical calculations and simulations of the FLR indicated that excitation energy transfer among PSIIs also affect the photochemical phase of the FLR (Lavergne and Leci 1993; Stirbet et al. 1998; Laz ar 2003; Zhu et al. 2005). II.4.1.4 Electric voltage across thylakoid membranes Using simultaneous recordings of the FLR and absorbance changes at 515 nm (A515 , reecting electric voltage across thylakoid membranes), Schreiber and Neubauer (1990) found that A515 has a maximum (there is a maximum in light-induced electric voltage across thylakoid membranes) approximately at the position of the J step. Schreiber and Neubauer (1990) suggested that the electric voltage favours formation of P680 triplet excited state (3 P680*). Formation of 3 P680* as such may lead to lower uorescence emission but energy of 3 P680* can be further quenched either in RCII or in LHA; this may lead to uorescence quenching at the J step. Similarly, using different frequencies of sinusoidal modulation of light source intensity, Dau et al. (1991) found that a time constant of uorescence signal equals a time constant of A520 , showing that the uorescence signal increases when electric voltage across thylakoid membrane
increases. Subsequent analysis of the measured data revealed that formation of electric voltage across thylakoid membrane is responsible for 7% of the photochemical phase of FLR (Dau et al. 1991). II.4.1.5 Electron transport through the inactive branch in PSII Schreiber (2002, 2004) has discussed a hypothetical mechanism to be responsible for the uorescence quenching at the J step. He proposed that in PSII with QA , an electron transport through the inactive branch in PSII can occur, that is, an electron may be transferred from P680 to Pheo localised in D2 protein of PSII (Pheo2) followed by an electron transport from the reduced Pheo2 to QB or QB . The proposed P680 Pheo2 QB (QB ) electron transport is assumed to be highly inefcient due to high yield of back non-radiative recombination. The proposed electron transport as such and the assumed high yield of back nonradiative recombination cause a uorescence quenching at the J step, which results in uorescence at the J step being smaller than at the P step of the FLR. Although it has already been shown that QB can be reduced via the inactive branch in mutants of anoxygenic photosynthetic bacteria Rhodobacter capsulatus and Rhodobacter sphaeroides (Kirmaier et al. 2003; Breton et al. 2004; Wakeham et al. 2004; Frolov et al. 2005; Paddock et al. 2005), a consideration of the inactive branch to affect the J step of the FLR as described above was only hypothetical. As QB is involved in the mechanism mentioned above, it was also called the QB -quenching mechanism (Schreiber 2002). However, further mechanisms in which QB is involved can be also called QB -quenching mechanisms as Schreiber (2004) has discussed in more details. According to this view, il, ZS Kolber, and PG Falkowski, as the results of O Pr as described in section II.4.2.1, which, however, have not been accepted by others, may be considered as a manifestation of a QB -quenching mechanism. Further research is necessary to test this hypothesis. II.4.1.6 Recombination between PSII electron acceptors and donors Goltsev and co-workers (Goltsev and Yordanov 1997; Goltsev et al. 2003, 2005; Zaharieva and Goltsev 2003) used a phosphoroscope method and theoretical simulations of delayed uorescence (DF) and the FLR to study effects of recombinations between PSII electron acceptors and donors leading to DF detected in the range of 350 s5.5 ms (for review on DF see Tyystj arvi and Vass 2004). The authors found that the time at which the rst peak (denoted as I1 ) in the DF intensity appears, corresponds with the time of a maximal rate of the FLR during the OI phase measured under low intensity of exciting light (Goltsev and Yordanov 1997; Goltsev et al. 2003; Zaharieva and Goltsev 2003). The origin of the I1 in the DF is probably in recombination of QA
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with YZ + when QB is singly reduced (Goltsev and Yordanov 1997; Zaharieva and Goltsev 2003; Goltsev et al. 2005) and the lifetime of YZ + QA QB is determined by the rate of electron transport from QA to QB (Goltsev et al. 2005). II.4.1.7 Effects of other processes Laz ar (2003) made a detailed analysis of the FLR by means of theoretical simulations of the FLR. For these simulations, Laz ar used a model that was obtained by combination of three existing models for the description of energy and electron transport steps in PSII: (i) the reversible radical pair (RRP) model (Breton 1983; van Grondelle 1985; Schatz et al. 1988; Leibl et al. 1989; Roelofs et al. 1992) describing energy utilisation leading to primary photochemistry, i.e. charge separation, recombination, and stabilisation (see Dau 1994 for a review); (ii) the model of Kok et al. (1970) describing the function of the donor side of PSII, i.e. that the Mn cluster of OEC undergoes a cycle through its four S-states; and (iii) the two-electron gate model (Bouges-Bocquet 1973; Velthuys and Amesz 1974; Crofts and Wraight 1983) describing the function of the acceptor side of PSII, i.e. that QB , unlike QA , is a two-electron acceptor. Therefore, this model (almost) completely included reactions on both the donor and the acceptor side of PSII. By changing values of particular rate constants or initial concentrations of states in the model, theoretical simulations by Laz ar (2003) indicated that the photochemical phase of the FLR is also affected by non-photochemical uorescence quenching by P680+ and by oxidised PQ pool, by charge recombination between P680+ and QA , by initial state of OEC, and by rate of electron transport from YZ to P680+ (for further details, see Laz ar 2003). Theoretical simulations by other authors also produced similar results (Stirbet et al. 1998; Zhu et al. 2005). II.4.1.8 The QB -reducing / non-reducing heterogeneity of PSII All previous explanations were made assuming PSII to be homogeneous. However, it is well documented in the literature that heterogeneity of PSII exists (reviewed by Lavergne and Briantais 1996). One type of the PSII heterogeneity is with respect to the ability of PSII to reduce QB . In this way PSIIs can be divided into two parts: (i) PSIIs that can reduce QB , the QB -reducing PSII, and (ii) PSIIs that cannot reduce QB , the QB -non-reducing PSII (Graan and Ort 1984, 1986; Whitmarsh and Ort 1984; Melis 1985; McCauley and Melis 1987; Chylla and Whitmarsh 1989; Lavergne and Leci 1993). With respect to this type of PSII heterogeneity, the photochemical phase was found to reect accumulation of QA of the QB -reducing but also ar et al. of the QB -non-reducing PSIIs (Hsu 1992a, b; Laz 1997b; Strasser and Stirbet 1997; Tomek et al. 2001, 2003; Laz ar 2003).
II.4.2 The thermal phase II.4.2.1 Accumulation of reduced QB in addition to reduced QA According to the suggestion by Delosme (1967), the thermal phase (JIP transient) corresponds to the destruction of a quencher R. Using present notations, R should be PQ, either bound to PSII as QB or free in thylakoid membranes. In agreement with this suggestion, as in the case of the photochemical phase of the FLR (see section II.4.1.1), Strasser and Govindjee (1992) suggested a working hypothesis proposing that the I and P steps reect light-driven accumulation of QB and QB 2 , respectively, in addition to the accumulation of QA , that is, I QA QB state and P QA QB 2 state. Although an accumulation of particular redox forms of PSII at the time of the appearance of the I and P steps in the FLR was conrmed only by theoretical simulations (Stirbet and Strasser 1995a, b, 2001; Stirbet et al. 1995, 1998; Laz ar et al. 1997b; Strasser and Stirbet 2001; Tomek et al. 2001; Lebedeva et al. 2002; Laz ar 2003; Zhu et al. 2005), assignment of the I and P steps to the redox forms seems to be reasonable, at least as the rst approximation. Even if several different models were used for the simulations, their results are, in general, the same as for the accumulation of particular redox forms. In agreement with the above-mentioned interpretation of il, ZS Kolber, the FLR are the unpublished results of O Pr as and PG Falkowski, obtained by site-directed mutants of the green alga Chlamydomonas reinhardtii, with substitution of Ala251 in the QB -pocket of the D1 protein, which affects the afnity of the PQ molecules for D1. These unpublished data may suggest that the thermal phase of the FLR is related to occupancy of the QB -site by the PQ molecule and by a capacity of QB to deoxidise QA (see also Samson et al. 1999). In agreement with this hypothesis, Yaakoubd et al. (2002) found, by measuring FM induced by a single turnover ash or by continuous illumination with samples treated with DCMU and exogenous PQs, that oxidised QB is responsible for 56% of the thermal phase of the FLR. II.4.2.2 Protonation of QB 2 Consistent with the explanation given in the previous section are the results of Heredia and De Las Rivas (2003), using PSII membranes treated with 1,4benzenediol (hydroquinone, HQ) and with 1,4-benzenedione (p-benzoquinone, PBQ). Heredia and De Las Rivas found that the addition of reduced and protonated quinones (HQ, PBQH2 ) resulted in uorescence quenching of the very last part of the thermal phase of the FLR. As they used PSII membranes for the measurements, which do not show the I step in FLR (see section II.3), they labelled the uorescence level that is unquenched by the quinones as the H level. However, this H uorescence level seems to be
16
D. Laz ar
different from the H step (peak) described in section III.2 and from a hump H described in section II.4.2.12. Heredia and De Las Rivas interpreted the JH transient to represent the reduction of QB to both QB and QB 2 and the HP transient to represent the protonation of QB 2 . An effect of protonation of QB 2 was also considered in theoretical simulations of the FLR (Laz ar et al. 1997b; Stirbet et al. 1998). II.4.2.3 The donor side of PSII An inhibition of the donor side of PSII suppresses the thermal phase of the FLR (Schreiber and Neubauer 1987; il and Dau 2000; Bukhov et al. 2004). A partial Posp s inhibition of OEC, caused either by various treatments that deplete components on the donor side of PSII, or high temperature treatment of PSII membranes (which lack the I step; see section II.3), led to a correlation between a rate constant of the JP transient of the FLR (see section II.3) il and and a steady-state rate of oxygen evolution (Posp s Dau 2000). Since a partial inhibition of the acceptor side of PSII, caused by addition of subsaturating concentrations of DCMU, resulted in a correlation between the rate constant and the steady-state rate of oxygen evolution too, the rate constant of the JP transient may be considered an indicator of the extent of electron ow from water to PQ il and Dau 2000). An effect of molecules generally (Posp s the inhibition of OEC on the thermal phase of the FLR was also revealed from theoretical simulation of the FLR (Laz ar 2003). Participation of the donor side of PSII in the JI phase of the FLR was discussed by Vredenberg et al. (2005) on the basis of a theoretical analysis of the three-state trapping model (TSTM) formulated by Vredenberg (2000) [see also Strasser and Stirbet (2001); Vredenberg (2004)]. In the TSTM, the open (PheoQA ), semi-open(closed) (PheoQA ), and closed (Pheo QA ) states of RCIIs are dened. A smaller rate constant of P680+ reduction by YZ in the higher S-states of OEC [summarised by Laz ar (2003)] results in a lower efciency of closing of the semi-open RCIIs that leads to a slow FLR during the JI phase (Vredenberg et al. 2005). II.4.2.4 Fluorescence quenching by the oxidised PQ pool As inhibition of OEC leads to a lack of electrons for the reduction of the PQ pool, the pool remains oxidised, and acts as a uorescence quencher (Vernotte et al. 1979; Hsu and Lee 1995; Kramer et al. 1995; Kurreck and Renger 1998; Kurreck et al. 2000; Haldimann and Tsimilli-Michael 2005). This uorescence quenching by the oxidised PQ pool is suggested to lead to the suppression of the thermal phase il and Dau 2000; Bukhov et al. 2004). Also using (Posp s the pump and probe method and ash uorescence induction measurements, the thermal phase was suggested to reect the removal of the uorescence quenching by the oxidised
ek et al. 2001). PQ pool (Samson and Bruce 1996; Kobl z However, measurement of FM , induced by single turnover ash or by continuous illumination, in samples treated with DCMU and by exogenous PQs, revealed that uorescence quenching by the oxidised PQ pool is responsible for only 25% of the thermal phase of the FLR (Yaakoubd et al. 2002). Therefore a question arises as to which part of the FLR reects the uorescence quenching by the oxidised PQ pool. As DCMU and chemicals that accept electrons from the acceptor side of PSI (both keep the PQ pool oxidised) suppress the IP phase of the FLR, it is the IP phase that reects uorescence quenching by the oxidised PQ pool (Neubauer and Schreiber 1987; Schreiber et al. 1989). An effect of the uorescence quenching by oxidised PQ pool on the FLR generally was also considered in theoretical simulations of the FLR (Stirbet et al. 1998; Laz ar 2003; Zhu et al. 2005). T oth et al. (2005) have recently found that if intact leaves are treated with DCMU carefully, the FM level is the same in the DCMU-treated leaves as in the controls (i.e. untreated leaves). This fact implies that the FM level is not sensitive to the redox state of the PQ pool and also that removal of the uorescence quenching by the oxidised PQ pool, as discussed above, is not responsible for the thermal phase of the FLR, at least in intact leaves. As discussed by T oth et al. (2005), the FM level is lowered in leaves treated with DCMU by a not-so-careful procedure because the treatment probably causes a damage of PSII enabling a better contact of oxidised PQ molecules from the pool with excited chlorophyll molecules in LHA. Therefore, T oth et al. (2005) suggested that extent of the PQ pool quenching expressed as lowering of the FM level could provide a tool to access the intactness of the PSII protein complex and quality of the isolation procedure used. II.4.2.5 The Q2 component Samson and Bruce (1996) suggested that the thermal phase of the FLR could also reect a reduction of a component, labelled as Q2 . The term Q2 was rst used by Joliot and Joliot (1977, 1979) as a putative electron acceptor, which needs more than one ash to be reduced in the presence of DCMU; it was part of an alternative electron pathway of very low quantum efciency. However, instead of dening the putative electron acceptor, Lavergne and Rappaport (1998) suggested that measured data can be explained by charge recombination between P680+ and QA . Nevertheless, consideration of the charge recombination had almost no effect on the simulated thermal phase of the FLR (Laz ar 2003). II.4.2.6 Cytochrome b559 Laz ar et al. (2005b) experimentally showed that an increase of the amount of initially reduced cytochrome (cyt) b559 in DCMU-treated thylakoid membranes resulted in an increase of the FM level. Theoretical simulations, where cyt b559 was assumed to accept electrons from Pheo and donate
17
electrons to P680+ (in the presence of DCMU), further supported this experimental nding. Therefore, with respect to denition of the Q2 component, as mentioned above, such a cyt b559 could be identied as the Q2 component. The reduced Pheo from work of Laz ar et al. (2005b) need not be the Pheo localised in the D1 protein of PSII but it can be Pheo2 localised in the D2 protein of PSII, which is a part of the inactive electron transport branch in PSII (see section II.4.1.5) and is closer to cyt b559 than Pheo in D1 as known from the structure of PSII (Zouni et al. 2001; Kamiya and Shen 2003; Ferreira et al. 2004). Further, Schreiber and Neubauer (1987) had suggested that if uorescence quenching by P680+ (Butler 1972; Mauzerall 1972; Sonneveld et al. 1979; Deprez et al. 1983; Shinkarev and Govindjee 1993; Bruce et al. 1997) causes quenching of uorescence signal at the J step, the reduction of P680+ by an alternate electron donor, e.g. by cyt b559 or a carotenoid, could result in uorescence increase during the thermal phase of the FLR. II.4.2.7 Fluorescence quenching in light harvesting antennae On the basis of measurements of uorescence decays after an application of single or multiple turnover ash, and tting of the experimental data by a model, Vasilev and Bruce (1998) suggested that removal of the uorescence quenching in LHA of PSII is responsible for the thermal phase of the FLR. Moise and Moya (2004a, b) reached a similar conclusion on the basis of their phase and modulation uorometry measurements: variable and transitory uorescence quenching occurs during the thermal phase, and the quenching results from a conformational change in a LHA of PSII and the LHA of PSII, where the conformational changes occur is CP47. II.4.2.8 Changes in yield of delayed (recombination) uorescence Schreiber and Krieger (1996) suggested another interpretation for the thermal phase of the FLR. These authors assumed that uorescence signal during the FLR consists of both the prompt uorescence and DF, the former originating directly from the excited states and the latter indirectly after the formation of the excited states, via radiative charge recombination between P680+ and Pheo (nanosecond range; for review on DF see Tyystj arvi and Vass 2004). Schreiber and Krieger (1996) further suggested that a gradual removal of non-radiative loss of the charge-separated state occurs in PSII in the P680+ Pheo QA state resulting in an increase of the yield of DF that leads to an increase of uorescence signal during the thermal phase of the FLR. The origin of changes in the DF was discussed by the authors to be connected to changes in positive charges stored at the donor side of PSII.
Goltsev and co-workers (Goltsev and Yordanov 1997; Zaharieva and Goltsev 2003; Goltsev et al. 2003, 2005) studied an effect of recombinations between PSII electron acceptors and donors by a phosphoroscope method and theoretical simulations of the DF and FLR (see section II.4.1.6). The authors found that the time at which the second peak (denoted as I2 ) in the DF intensity appears, corresponds with the time of a maximal rate of the FLR during the IP phase measured under low intensity of exciting light (Goltsev and Yordanov 1997; Goltsev et al. 2003; Zaharieva and Goltsev 2003). The origin of the I2 in the DF is probably in recombination of QA with YZ + when QB is doubly reduced (Goltsev and Yordanov 1997; Zaharieva and Goltsev 2003; Goltsev et al. 2005) and the lifetime of YZ + QA QB 2 is determined by the sum of the rate constants of electron transport from the S-state transitions of OEC to YZ + and of exchange between the reduced and oxidised PQ molecules in the QB -site of PSII (Goltsev et al. 2005). II.4.2.9 Electron transport reactions after PSII When the FLR is measured, in the green alga Chlorella, under low intensity of excitation light, a dip D usually appears after the I step (Munday and Govindjee 1969a). It was suggested that appearance of the dip is related to function of PSI (Munday and Govindjee 1969b; Schreiber et al. 1971; Satoh and Katoh 1981; Hansen et al. 1991). However, using theoretical modelling of the FLR measured under low intensity of excitation light, Baake and Strasser (1990) and Baake and Schl oder (1992) showed that inclusion of electron transport reactions occurring after the PQ pool [cyt b6 / f complex, plastocyanin (PC), PSI] in a model does not improve a t of the model to a part of the FLR around the position of the dip D of the experimental FLR curves measured with leaves. Also other authors assumed the electron transport reactions occurring after the PQ pool in theoretical simulations of the FLR (Goltsev and Yordanov 1997; Lebedeva et al. 2002). New information about the electron transport chain after the PQ pool has been obtained by simultaneous measurement of the FLR and transmission changes at 820 nm (T820 ), which should reect changes in redox state of PC and P700. Schreiber et al. (1989), R. J. Strasser and co-workers (Strasser et al. 2001; Schansker et al. 2003, 2005) showed that T820 has a minimum exactly at the position of the I step in the OJIP FLR measured with leaves. On the basis of 2,5-dibromo-3-methyl-6-isopropylp-bezoquinone (DBMIB) and methylviologen (MV) action on the FLR and T820 signal, Schansker et al. (2005) suggested that a transient limitation at the acceptor side of PSI leading to a trafc jam of electrons transiently formed in the electron transport chain are responsible for the IP transient of the FLR (cf. Munday and Govindjee 1969b). It is likely that this limitation on the PSI side can be rst caused by inactive ferredoxin-NADP+ oxidoreductase
18
D. Laz ar
(FNR) and consequently by the inactive CalvinBenson cycle (Schansker et al. 2003). II.4.2.10 Fluorescence coming from PSI Observations of direct uorescence from PSI has been recently reviewed by Itoh and Sugiura (2004). Here, I present a discussion of the effect of PSI reactions on OJIP FLR. Applying saturating light pulses of varying lengths and measuring the T820 signal with leaves treated with MV and using far-red background illumination (to avoid any limitation at the acceptor side of PSI), Schreiber et al. (1989) found that the electron transport chain is reduced within 50 ms; that is at a time when the I step appears in the FLR. On the basis of this result and of measured changes in the T820 signal, as mentioned above, the IP transient in the FLR was suggested to reect a reduction of P700 and of PSI acceptor side caused by a limitation at the acceptor side of PSI (Munday and Govindjee 1969b; Schreiber et al. 1989). Further, Ikegami (1976) found that when P700 is reduced by dithionite in P700-enriched particles, the particles upon illumination (by blue light) showed an increase in uorescence signal (detected at 694 nm) at room temperature. This result together with the suggestion mentioned above led Ulrich Schreiber and co-workers (Schreiber et al. 1989; Schreiber 2002) to suggest that the IP transient of the FLR could reect an increase in uorescence signal coming from PSI. More recently, Byrdin et al. (2000) also found that the trimeric PSIs with initially reduced PSI by ascorbate (i.e. P700 being initially present) show a FLR (excited by HeNe laser at 633 nm and detected at wavelengths above 665 nm) at room temperature with variable uorescence FV (= FM F0 ) equal to 12 5% of FM . However, to prove that the IP transient of the FLR reects exclusively uorescence signal coming from PSI, direct comparison of the FLRs measured at different emission wavelengths is necessary. II.4.2.11 Light gradient within a sample As any photosynthetic sample used for measurements of the FLR curves represents layers of pigments, a light gradient within the sample, in addition to other optical effects, is created along the light path. The gradient then results in the excitation of particular sub-layers of the sample by light of different intensities and the detected overall uorescence signal is a sum of the signals coming from the sub-layers. Assuming this simple rationale and using different sample preparations, Hsu and Leu (2003) suggested that the I step in the FLR originates in the abaxial layer(s) of the sample (when it is illuminated from the adaxial side). As it is the photochemical phase of the FLR that is very sensitive to the intensity of exciting light (see section II.2), the I step in the overall FLR should in fact reect the photochemical phase of the FLR coming from the abaxial layer(s) of the sample (Hsu and Leu 2003).
Franck et al. (2005) also suggested a participation of uorescence signals coming from particular layers of the sample to overall uorescence signal of the FLR on the basis of measurements of uorescence emission spectra at room temperature during the FLR with different samples and using theoretical simulations of the spectra. On the basis of the theoretical simulations, Franck et al. (2005) also concluded that as the time elapses from the onset of excitation, the measured uorescence signal during the FLR originates from deeper layers. Even though an effect of the light gradient within the sample on the overall FLR was explored by both experimental measurements and theoretical simulations (Su sila et al. 2004), it was not proven that the light gradient is responsible for the appearance of the I step in the FLR. However, if the FLR is used as an analytical tool to access information about photosynthetic function, care must be exercised in interpreting the data (Hsu and Leu 2003; Su sila et al. 2004). Su sila et al. (2004) surmised that the light gradient within the sample can signicantly affect the results of the JIP test (see section V .1) mainly in the case when the concentration of Chls is changed when a plant is stressed. II.4.2.12 Electric voltage across the thylakoid membrane When the FLR is measured with PSII membranes the I step is missing in the FLR, in contrast to more intact samples where the I step is present (see section II.3). However, PSII membranes do not form closed compartments, which would enable the formation of electric voltage across the membrane. These facts, together with the existing coincidence in the times of the I step appearance in the FLR (at 3050 ms) and the formation of a peak in light induced electric voltage across the thylakoid membrane (at 2050 ms but with different samples, for reviews see Bulychev and Vredenberg 1999; Vredenberg 2004), led il and Dau (2002) to suggest that the I step reects Posp s light induced changes in electric voltage across thylakoid membranes. Application of valinomycin with potassium ions, led to a short-circuit with respect to the membrane voltage and the I step disappeared from the FLR measured with thylakoid membranes. Similarly the appearance of a hump, labelled as H (note: this hump is different from the H uorescence level described in section II.4.2.2.2 and from the H peak described in section III.2), in the FLR but measured under low intensity of exciting light with Bryopsis chloroplasts was related to changes in light-induced membrane voltage (Satoh and Katoh 1981). However, appearance of the I step in FLR and a peak in light-induced electric voltage across thylakoid membranes in the same time as assumed by Pospil and Dau (2002) is in contrast to results of Schreiber and Neubauer (1990), who found that the light-induced electric voltage across thylakoid membranes has a maximum at the J step and not at the
19
I step of the FLR (see section II.4.1.4). Further, Schreiber and Neubauer (1990) suggested that increase of uorescence signal during the thermal phase of the FLR reects a lowering of uorescence quenching driven by a relaxation of the membrane voltage, where the uorescence quenching occurs by a mechanism as described in section II.4.1.4. In addition to the participation of 3 P680* as described in section II.4.1.4, there are two other mechanisms related to changes in electric voltage across thylakoid membranes that affect changes in uorescence emission directly and indirectly. In the direct mechanism, formation of the electric voltage causes a decrease in Gibbs free-energy difference, G0 , between the excited states in RCII and the charge separated state (P680+ Pheo ): the decrease in G0 leads to a decrease in the rate constant of primary charge separation and increase in the rate constant of primary charge recombination, both resulting in an increased accumulation of excited states leading to increased uorescence emission (Dau et al. 1991; Dau and Sauer 1991, 1992). In connection to the indirect mechanism, Graan and Ort (1983) found that a marked stimulation of the electron transport rate occurred when chloroplasts were treated with valinomycin, and they explained this effect by an increased rate of plastoquinol oxidation. Therefore, when valinomycin is not present a light-induced electric voltage across the thylakoid membrane is formed, causing a decrease in the rate of plastoquinol oxidation that leads to an increased accumulation of reduced QB and QA that results in an increased uorescence emission. Similarly, Goltsev and Yordanov (1997) assumed a decrease in the rate constant of plastoquinol oxidation caused by an intra-thylakoid space acidication in theoretical simulations of the FLR. It is evident from the above text that both the direct and the indirect mechanisms involve changes in the rate constants of electron transport steps. Therefore it is clear that when a light-induced electric eld is present, rate constants of all the electron transport steps will be changed and will somehow contribute to changes in uorescence emission. Such an approach was used by Lebedeva et al. (2002), who assumed a dependence of the rate constants of all the electron transport steps in thylakoid membranes on the light-induced electric voltage across thylakoid membranes in theoretical simulations of the FLR. An effect of electrogenic events across thylakoid membranes on the FLR has been extensively studied by WFJ Vredenberg and AA Bulychev (Bulychev and Niyazova 1989; Vredenberg 2000; Bulychev and Vredenberg 2001; Vredenberg and Bulychev 2002, 2003). Bulychev and Vredenberg (2001) found that electrogenic events generated in PSI, when PSII photochemical activity was absent (caused by NH2 OH treatments), affect the PSII. Thus, Vredenberg and Bulychev (2002) suggested the so-called the photoelectrochemical control of uorescence yield: when the photochemical activity of PSII is absent at the I step of
the FLR (assuming that all the electron acceptors in PSII are already reduced), the subsequent IP transient is due to changes in uorescence yield caused by electric events across the thylakoid membrane (see also Vredenberg 2004). An effect of light induced changes in pH or the electric voltage across thylakoid membrane was also included in models, which simulated FLR curves for different intensities of exciting light (Goltsev and Yordanov 1997; Lebedeva et al. 2002). II.4.2.13 The heterogeneity in the rate of PQ pool reduction All the explanations, thus far discussed in this review, were made assuming PSII to be homogeneous. As already mentioned above (see section II.4.1.8), PSII is heterogeneous in many aspects. One aspect of the PSII heterogeneity is in the rate of reduction of particular PQ pools (Joliot et al. 1992; Kirchhoff et al. 2000). In addition to a fast-reduced PQ pool localised mainly in thylakoid grana, there also exists a slowly reduced PQ pool localised mainly in stromaexposed thylakoid membranes. To incorporate this type of heterogeneity into explanation of the FLR, the JI and IP transients of the thermal phase were suggested to reect a reduction of the fast and slow PQ pool, respectively (Strasser et al. 1995; Barth elemy et al. 1997; Schreiber 2002). Further, Bukhov et al. (2003) found that addition of a weak concentration of N,N,N ,N -tetramethyl-p-phenylenediamine (TMPD) leads to a clearer appearance of the I step in the FLR measured with thylakoid membranes. Since Bukhov et al. (2003) used TMPD as an electron acceptor from the reduced PQ pool (see also Joly et al. 2005), the resolution of the I step resulted from a decreased reduction of both fast and slowly reducing PQ pool. Similarly, theoretical simulations of the FLR revealed that assuming a slowly reducing PQ pool in a model leads to an appearance of a step in the thermal phase of the FLR (Laz ar 2003). II.4.3 A summary The results presented in the previous sections suggest that many events may affect the nal shape of measured FLR. Some of the conclusions were based on precise experiments and their detailed analyses but some of them were only from hypotheses. It is not yet possible to say denitively which mechanisms really (or only) contribute to the nal shape of the FLR and which do not. It is highly likely that all the mechanisms mentioned contribute to the FLR to some extent. One way to quantify the extent by which a particular mechanism contributes to a measured quantity is to form a mathematical model describing all the involved mechanisms and evaluate the extent to which a mechanism contributes to the measured quantity by means of exact mathematical formulae. Such an approach is common in mathematical modelling of metabolic pathways and is known as metabolic
20
D. Laz ar
control analysis [MCA; for reviews on MCA, see Fell (1992); Visser and Heijnen (2002)]. In MCA, in addition to other coefcients, the control coefcient C, which exactly quanties the extent to which a particular model parameter (concentration or activity or rate constant) controls a selected variable of the model (concentration or ux), is calculated. MCA has already been used for exploration of several plant metabolic pathways, e.g. the CalvinBenson cycle (Poolman et al. 2000) and the malate valve (Fridlyand et al. 1998), but it has also been used for exploration of uorescence data related to photosynthetic function; a simple MCA-like method was used for the analysis of changes in oscillations in steady-state uorescence signal caused by high temperature treatment (Laz ar et al. 2005c) and MCA was used for the analysis of changes in FM of the DCMU-FLRs due to changes in initial redox state of cyt b559 (Laz ar et al. 2005b; see section II.4.2.6). Therefore, it is a challenge for future work to construct a mathematical model of the FLR, which would include all suggested mechanisms and evaluate contributions of particular mechanisms to FLR by means of MCA. III The K, H, and G steps in the uorescence rise III.1 The K step When samples are treated with high temperature, a new step at 300400 s, denoted as K, appears in FLR (Guiss e et al. 1995a, b; Srivastava et al. 1997; Laz ar and Il k 1997; Laz ar et al. 1997a; Strasser 1997; see Fig. 2, curve b). Reto
Strasser and his co-workers (Guiss e et al. 1995a; Strasser 1997) suggested that the appearance of the K step reects an inhibition of OEC, probably together with an inhibition of the acceptor side of PSII (Laz ar et al. 1999). More generally, Strasser (1997) suggested that the K step arises when the rate of electron ow from P680 to the acceptor side of PSII exceeds the rate of electron ow from the donor side of PSII to P680. Srivastava et al. (1997) and il (1999) found that the appearance of Laz ar and Posp s the K step reects changes in the energetic connectivity between PSIIs. As the K step reects an accumulation of reduced QA (Strasser 1997), the OK rise is also the photochemical phase of FLR. However, the photochemical phase of the FLR measured at room temperature (the OJ transient) does not simply move to shorter times (the OK transient) when measured with high temperature treated samples because both the K and J steps can be measured together under certain conditions (Guiss e et al. 1995a, b; Srivastava et al. 1997; see Fig. 2, curve c). This fact suggests that the K and J steps might reect two different phenomena (Guiss e et al. 1995a, b; Srivastava et al. 1997). Therefore, the source of the K step is expected to be present even in unstressed samples but for dynamic reasons it does not appear as a clear step in the FLR (Guiss e et al. 1995a, b; Srivastava et al. 1997; Strasser 1997). The same conclusion can also be drawn from positions of peak accumulations of excited states simulated on the basis of a theoretical model of the FLR (Laz ar 2003). III.2 The H and G steps
Fluorescence intensity (relative units)
P H I
a G d
J K
P P c
O
1
O
4 3 2 1 0
Log time (s)

Fig. 2. Chlorophyll a uorescence rise measured with dark-adapted pea leaves (curve a, no treatment; curve b, leaf incubated at 47 C in water for 5 min), potato leaf (curve c, leaf incubated at 44 C in water for 13 min), and with lichen Umbilicaria hirsuta (curve d, no treatment) by PEA uorometer under high intensity of exciting light ar 1999 and [3400 mol photons m2 s1 of red light; data from Laz courtesy of P. Il k and M. Bart ak (curve d)]. The O, K, J, I, H, G, and P steps are labelled.
The OJIP FLR is not a typical property of all photosynthetic organisms under standard conditions. The P step, measured at high intensity of excitation light at room temperature, was found to be split into two steps in the FLR in foraminifers (Tsimilli-Michael et al. 1998a, b), zooxanthellae (Hill et al. 2004), lichens (Bukhov et al. 2004), and in lichens and lichenised algae (Il k et al. 2006; see Fig. 2, curve d). To continue with the previous OKJI notation, the two steps were labelled as H and G (Tsimilli-Michael et al. 1998a, b). On the basis of simultaneous measurements of FLR and T820 signal with different samples treated with different chemicals, Il k et al. (2006) found that uorescence decrease from the H step to a dip between H and G steps is caused by a removal of limitation on the acceptor side of PSI, probably caused by light-induced activation of FNR (see section II.4.2.9) or cyclic electron ow around PSI or Mehler reaction, resulting in a transient reoxidation of reduced PQ pool (and QA ). Following uorescence increase from the dip between H and G steps to the G step is then caused by subsequent PQ pool (and QA ) re-reduction. The PQ pool rereduction is not associated with cyclic electron ow around PSI and is probably caused by inability of the cyt b6 / f complex to rapidly reoxidise the PQ pool (Il k et al. 2006).
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In light of the discussion above, the H step mentioned here seems to be different from the H uorescence level and from the hump H described in sections II.4.2.2 and II.4.2.12, respectively. Thus, a different nomenclature is ultimately needed to describe this H step. IV Statistical properties of parameters determined from the uorescence rise IV .1 Presentation of parameters determined from the uorescence rise Statistical evaluation of FLR data is not routine in the literature and when it is used, it is only to fulll standard requirements for the data presentation. The values of F0 , FM , FV / FM parameters [and also other uorescence parameters (FPs) determined from FLR] are very often presented by means of the mean and standard deviation (or standard error) in the literature (see e.g. Bj orkman and Demmig 1987). But to present any parameter by means of the mean and standard deviation (or standard error), the distribution of the parameters data should be Gaussian. However, the FPs (F0 , FJ , FI , FM , FV , VJ , VI , FV / FM , etc.) generally do not have Gaussian distribution (Laz ar and Nau s 1998; Laz ar et al. 2003, 2005a, 2006). Therefore, presentation of data by means of the mean and standard deviation (or standard error) is not appropriate and it masks the real data distribution of the FPs. The use of median, quartiles, and maximal and minimal values better describes a real situation of data distribution (Laz ar and Nau s 1998). Further, because the FPs of the FLR generally do not have Gaussian distributions, the nonparametric test should be used for statistical comparisons of the FPs rather than the parametric tests, which are based on the assumption of Gaussian distribution of data. IV. 2 Changes in statistical distributions of uorescence parameters caused by stress Generally, statistical distribution (histogram) of a FP, measured under non-stressed conditions, is not Gaussian but skewed to a side (Laz ar and Nau s 1998; Laz ar et al. 2003, 2005a, 2006). When plant material suffers from stress, changes in statistical distributions of the parameters occur and these changes depend on the extent of the stress. For example, the FM level, measured with barley leaves upon high temperature treatment, is skewed to the left for measurements at room temperature (i.e. most of the FM values are high, on the right in the histogram, but there are also some smaller FM values, on the left in the histogram), then symmetrical (44 C), then skewed to the right (51 C), ar et al. 2005a). and nally symmetrical again (65 C) (Laz The observed changes in distributions of FM can be well explained in the sense of changes in functional heterogeneity of PSIIs, assuming that a stress leads to a malfunction of PSII and causes a decrease in the FM level (Laz ar et al. 2005a). However, complete changes in the distributions as described above can be observed only when plant material
suffers progressively from weak to severe stress (Laz ar 2005): when a stress is not severe, not all stages of change in the distribution can be observed, as was the case for measurement with pumpkin leaves that suffered from senescence and fungal infection (Laz ar and Nau s 1998) or with wheat leaves that suffered from senescence and other stresses (Laz ar et al. 2003). Changes in distributions of FPs, determined from FLR, caused by stress, as described above, are also accompanied by changes in variances of measured data and the changes in variances are different for different FPs (Laz ar et al. 2003, 2005a). The different variances of the FPs can be indicative of different processes described by the FPs (Laz ar et al. 2005a). The difference in variances of the FPs can be used for an evaluation of mutual independence of two FPs and, thus, also of mutual independence of processes described by the FPs (Laz ar et al. 2003, 2005a). For example, it was found, for the case of a high temperature stress, that for almost all combinations of two basic FPs (F0 , FK , FJ , FI , FM ), there is an increase in mutual independence of the FPs in the temperature range 4451 C and therefore also an increase in mutual independence of processes characterised by the FPs in this temperature range (Laz ar et al. 2005a). Laz ar et al. (2006) showed that a detailed analysis of changes in statistical distributions of FPs could be useful for early detection of plant stress. To obtain a large amount of experimental data for a given FP (necessary for detailed analysis), they measured FI with leaf segments under a low intensity of exciting light with an imaging uorometer. Selected FP of control (no stress) and stressed samples (stress mainly by a dehydration of the segments in this work) were compared by classical statistical comparison (Mann-Whitney test; compares values of the medians) and by statistical comparison of shapes of distributions of the FPs (two-sample Smirnov test). The authors found that examples exist in which statistically signicant difference is not revealed by the classical statistical comparison (for given critical level) but statistically signicant difference is revealed by comparisons of distributions (for the same critical level). It implies that the shape of statistical distribution of a FP is more sensitive to stress than the median of the FP and that the comparison of changes in shapes of statistical distributions of FPs is therefore more suitable for early detection of plant stress than a classical statistical comparison (Laz ar et al. 2006). V Applications of the uorescence rise V .1 The JIP test for the so-called vitality screening With the main goals to measure several hundreds of samples per hour and to provide a manual that non-specialists can execute the measurements and obtain results in a standard form, a test, known as the JIP test, was formulated by Strasser and Strasser (1995) for vitality screening
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upon changing environmental conditions. The test was later produced as a free software Biolyzer (Laboratory of Bioenergetics, University of Geneva, Switzerland; http://www.unige.ch/sciences/biologie/bioen/jipsoftware. html; veried 12 September 2005). The basis of the test is measurement of the FLRs with PEA uorometer followed by an analysis of measured curves. In this JIP test, basic parameters evaluated from the FLR curves, such as F0 , FM , uorescence signals at 100 and 300 s and at the J, I and P steps, are used for subsequent calculation of different parameters that are somehow related to energy and electron uxes in PSII and therefore to photosynthetic function generally (see Strasser et al. 2004). The JIP test seems to be very popular now; when a search term jip and test and uorescence was used in the Web of Science search engine, 31 articles were listed (search performed on 7 July 2005) published during a period from 1997 to 2005. For example, choosing only from ten of the most recently published articles, the JIP test was used for study of effects of ambient v. reduced UV-B radiation on Salix arctica plants (Albert et al. 2005), comparison of ozone foliar symptoms in woody plant species (Bussotti et al. 2005), quantication of the photosynthetic performance of phosphorus-decient Sorghum plants (Ripley et al. 2004), assessment of stress conditions in Quercus ilex L. leaves (Bussotti 2004), description of effect of salinity stress on PSII in Ulva lectuca (Xia et al. 2004), exploration of low temperature tolerance of tobacco plants (Parvanova et al. 2004), exploration of ozone action on Mediterranean evergreen broadleaves and on woody plant leaves (Paoletti et al. 2004; Gravano et al. 2004), phenotyping of dark- and lightadapted barley plants (Oukarroum and Strasser 2004), and detection of draught and salinity tolerance chickpea varieties (Epitalawage et al. 2003). Although the JIP test is very often used now, the results should be taken with care, especially in the case when the concentration of Chls is changed during stress (Su sila et al. 2004; see section II.4.2.11). V.2 Remote sensing and pattern recognition in precise agriculture There is a rapidly growing interest for plant identication in agriculture practice with the aim of recognising cultivated plants from weeds. Then, using a sprayer mounted on a tractor, herbicides and other agrochemicals could be applied selectively and precisely. This approach would result in precision farming or precision agriculture, the terms that are used very often now. Precision agriculture requires a tool that enables remote sensing of the plants and simultaneous recognition. One way to determine the plant species is to measure FLRs, which are characteristic for given species and can be used as ngerprints. Application of sophisticated mathematical
procedures (the genetic algorithms and neural networks classiers) then would enable recognition of particular species on the basis of their ngerprints. Fluorescence signal can be also measured by a CCD camera from a large area (i.e. measurement of uorescence imaging; for reviews see Chaerle and Van Der Straeten 2000, 2001; Nedbal and Whitmarsh 2004; Oxborough 2004a, b), enabling fast and effective remote sensing (for a review see Moya and Cerovic 2004). Therefore, it seems that chlorophyll uorescence signal is the tool needed for precision agriculture. The rst results of the pattern recognition using uorescence techniques came from measurements of uorescence induction (FI) by a PAM uorometer (i.e. with low time resolution, but with both FLR and uorescence decay being measured). A special design of illumination routine, given to dark-adapted samples, consisted of application of red light of moderate intensity, far-red light, high intensity white light, and dark intervals (Tyystj arvi et al. 1999). However, this type of data collection required a long time, which conicts with the need for rapid data capture during tractor movement in eld conditions. Therefore, FLRs measured with leaves without dark adaptation and using a PEA uorometer were also used for subsequent analysis by the same research group (Ker anen et al. 2003). Importantly, the analysis based on the PEA data had about the same or, in some cases, even better accuracy of correct identication as the analysis based on the PAM data (Ker anen et al. 2003). When FLR or FI is used for pattern recognition, whole measured curves are not used but, instead, only some features of the curves are analysed. Currently, the features used are slopes and y-axis intercepts of regression lines to experimental FLR or FI data in selected time intervals. The best selection of the time intervals is therefore very important to obtain features that are species-specic and therefore usage of which would result in best pattern recognition. This problem was addressed by Codrea et al. (2003, 2004), who used an optimiser (genetic algorithm) to tune the endpoints of the time intervals to improve the pattern recognition. V.3 In silico photosynthesis to understand photosynthetic regulations and limitations future prospects A summary of possible origins of the steps in the FLR, given in sections II.4 and III, clearly shows that there exist several regulatory mechanisms that can ne tune photosynthetic performance, even during the very rst second of illumination of photosynthesising organisms. What is important is that not only the function of PSII can be reected in the FLR but also a function of the electron transport chain within thylakoid membranes and a means of subsequent electron usage by FNR and the CalvinBenson cycle. Therefore, in principle, all the photosynthetic reactions, involved in different
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levels of organisation, should be somehow reected in the FLR or FI. Prolonged light illumination and consideration of higher levels of organisation lead to very large numbers of different regulatory mechanisms involved in different levels of organisation. One way to understand the complexity of operating machinery is to use mathematical modelling of all the events, i.e. to form in silico photosynthesis. Mathematical modelling is therefore an important tool for the better understanding of the explored processes. For recent reviews on mathematical modelling of plant metabolic pathways, see Giersch (2000) and Morgan and Rhodes (2002). At present there is no global model of photosynthesis (but see http://www.e-photosynthesis.org for a developing project; veried 12 September 2005) that would satisfactorily describe all the related phenomena measured by respective quantities. However, several detailed models describing particular photosynthetic events and regulations have been suggested. For example, in addition to exploration of the OJIP FLR, models describing electron transport reactions within thylakoid membrane were also used for theoretical exploration of the electron transport chain as such (Berry and Rumberg 2001), ash and continual light induced oxygen evolution (Ka na et al. 2002), dependence of uorescence signal on linearly increasing temperature of the sample (Kou ril et al. 2004), and forced uorescence oscillations (Nedbal et al. 2005). It is therefore a challenge for future work to construct a mathematical model of whole photosynthesis. Such model would be used, for example, in revealing the regulatory mechanisms that are not directly accessible or understandable from the available experimental data and for nding the limitations of photosynthesis under different experimental conditions. When limitations of photosynthesis under different conditions are found, they can be used in an effort to increase photosynthetic efciency and crop yield by means of specic mutations. However, engineering mutants, which lead to increased efciencies and yields, remains a long-term goal. Sinclair et al. (2004) showed, by means of theoretical calculations, that assumed 50% increase in mRNA production responsible for the synthesis of small and large subunits of ribulose-1,5bisphosphate carboxylase / oxygenase (Rubisco), the key enzyme in CalvinBenson cycle, would lead only to 37% increase in Rubisco content, 33% increase in light-saturated leaf photosynthetic rate, 30% increase in photosynthetic rate of isolated plant, 18% increase in accumulated crop mass, 6% increase in grain yield with additional nitrogen supply, but possibly a 6% decrease in grain yield without additional nitrogen supply. Therefore it seems that there may not be much room to increase efciency and yield of natural photosynthesis. Thus, efforts should be focused on the construction of an articial photosynthesis to serve our increasing consumption demands.
VI Conclusions This review has summarised the current understanding of the FLR measured under high intensity of exciting light, the OJIP transient. The review also included a discussion of other steps, K, H, and G, which appear in the FLR under certain conditions. Some specic applications of the FLR were also mentioned. Although as the current text implies, many interpretations have been suggested for the particular steps of the FLR, yet this phenomenon is not fully understood. Further research is necessary to fully understand the relationship of the OJIP transient to photosynthetic reactions. Acknowledgments This work was nancially supported by the Ministry of Education of the Czech Republic by a grant number MSM 6198959215. This review was also a part of the Habilitation Thesis of the author (Laz ar 2005). I thank Professors Govindjee, Ulrich Schreiber, and Reto J. Strasser for their valuable comments that have improved this presentation. In addition, Govindjee has also edited parts of the manuscript. References
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Manuscript received 19 April 2005, accepted 18 August 2005
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CSIRO PUBLISHING

Functional Plant Biology, 2006, 33, 930

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

Fluorescence intensity (relative units)

4 4 3 2 1 4 3 2 Log time (s) 1 2

Log time (s)

Fluorescence yield (relative units)

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

Fluorescence intensity (relative units)

Log time (s)

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

The polyphasic chlorophyll a uorescence rise

Functional Plant Biology

Functional Plant Biology

Manuscript received 19 April 2005, accepted 18 August 2005

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